Molecular adaptations to phosphorus deprivation and comparison with nitrogen deprivation responses in the diatom Phaeodactylum tricornutum

Abstract

Phosphorus, an essential element for all living organisms, is a limiting nutrient in many regions of the ocean due to its fast recycling. Changes in phosphate (Pi) availability in aquatic systems affect diatom growth and productivity. We investigated the early adaptive mechanisms in the marine diatom Phaeodactylum tricornutum to P deprivation using a combination of transcriptomics, metabolomics, physiological and biochemical experiments. Our analysis revealed strong induction of gene expression for proteins involved in phosphate acquisition and scavenging, and down-regulation of processes such as photosynthesis, nitrogen assimilation and nucleic acid and ribosome biosynthesis. P deprivation resulted in alterations of carbon allocation through the induction of the pentose phosphate pathway and cytosolic gluconeogenesis, along with repression of the Calvin cycle. Reorganization of cellular lipids was indicated by coordinated induced expression of phospholipases, sulfolipid biosynthesis enzymes and a putative betaine lipid biosynthesis enzyme. A comparative analysis of nitrogen- and phosphorus-deprived P. tricornutum revealed both common and distinct regulation patterns in response to phosphate and nitrate stress. Regulation of central carbon metabolism and amino acid metabolism was similar, whereas unique responses were found in nitrogen assimilation and phosphorus scavenging in nitrogen-deprived and phosphorus-deprived cells, respectively.

Absolute Quantification of the Central Carbon Metabolome in Eight Commonly Applied Prokaryotic and Eukaryotic Model Systems

“…This could mostly be attributed to high levels of Citrate (Cit) and aKG (Figure 5b, right panel). Other studies have implicated the TCA cycle and accumulation of Cit, specifically in the response to nutrient stress in this species [58,63], indicating that flux to and from Cit might be an important regulatory node in P. tricornutum.…”

“…Two sequenced model microalgal species, N. oceanica [56] and P. tricornutum [57], were included in the panel for metabolite profiling. Due to ease of genetic manipulation and high yield of nutritionally beneficial polyunsaturated fatty acids, these species are gaining interest for industrial applications [56,58,59].…”

A novel Ca2+signalling pathway co-ordinates environmental phosphorus sensing and nitrogen metabolism in marine diatoms

“…We also observed significant enhancement of phosphate acquisition and recycling proteins in P limited versus P replete cells (Alipanah et al, 2018; Cruz de Carvalho et al, 2016). Indeed, under P limitation, the four most highly-expressed proteins included a glycerophosphoryl diester phosphodiesterase and three predicted alkaline phosphatases ( Dataset S3 ).…”

“…Our work also highlights that fundamental cross-talk between the essential nutrients phosphorus and nitrogen drive ecological acclimation to phosphorus availability in diatoms. Phosphorus-limited cells invest primarily in phosphate acquisition (Alipanah et al, 2018; Cruz de Carvalho et al, 2016), scavenging (Dyhrman et al, 2012; Ly et al, 2014) and reallocation (Martin et al, 2011), diverting resources away from vital processes such as nitrogen assimilation. Meanwhile, activation of the phosphate-Ca 2+ signalling machinery readies cells for detection of phosphorus resupply, which governs rapid phosphate-driven induction of nitrogen-assimilation proteins.…”

“…Upregulation of phosphate transporters is well-documented (Cruz de Carvalho et al, 2016). Moreover, enhanced expression of alkaline phosphatases and/or phosphodiesterases, increases phosphorus scavenging capacity (Alipanah et al, 2018; Cruz de Carvalho et al, 2016; Dyhrman, 2016; Dyhrman et al, 2012; Lin et al, 2013; Yang et al, 2014). Diatoms, and other phytoplankton, also substitute phospholipids with non-phosphorus forms to decrease cellular demand (Martin et al, 2011; Van Mooy et al, 2009).…”